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Original research
Histological evaluation of acute ischemic stroke thrombi may indicate the occurrence of vessel wall injury during mechanical thrombectomy
  1. Oana Madalina Mereuta1,2,
  2. Mehdi Abbasi1,
  3. Seán Fitzgerald1,2,
  4. Daying Dai1,
  5. Ram Kadirvel1,
  6. Ricardo A Hanel3,
  7. Albert J Yoo4,
  8. Mohammed A Almekhlafi5,
  9. Kennith F Layton6,
  10. Josser E Delgado Almandoz7,
  11. Peter Kvamme8,
  12. Vitor Mendes Pereira9,
  13. Babak S Jahromi10,
  14. Raul G Nogueira11,12,
  15. Matthew J Gounis13,
  16. Biraj Patel14,
  17. Amin Aghaebrahim3,
  18. Eric Sauvageau3,
  19. Parita Bhuva4,
  20. Jazba Soomro4,
  21. Andrew M Demchuk5,
  22. Ike C Thacker6,
  23. Yasha Kayan7,
  24. Alexander Copelan7,
  25. Pouya Nazari10,
  26. Donald Robert Cantrell10,
  27. Diogo C Haussen11,12,
  28. Alhamza R Al-Bayati11,12,
  29. Mahmoud Mohammaden11,12,
  30. Leonardo Pisani11,12,
  31. Gabriel Martins Rodrigues11,12,
  32. Ajit S Puri13,
  33. John Entwistle14,
  34. Alexander Meves15,
  35. Jorge L Arturo Larco1,16,
  36. Luis Savastano1,16,
  37. Harry J Cloft1,16,
  38. David F Kallmes1,16,
  39. Karen M Doyle2,
  40. Waleed Brinjikji1,16
  1. 1Department of Radiology, Mayo Clinic, Rochester, Minnesota, USA
  2. 2CÚRAM – SFI Research Centre for Medical Devices and Department of Physiology, National University of Ireland Galway, Galway, Ireland
  3. 3Department of Neurosurgery, Baptist Medical Center, Jacksonville, Florida, USA
  4. 4Department of Neurointervention, Texas Stroke Institute, Dallas-Fort Worth, Texas, USA
  5. 5Departments of Clinical Neurosciences, Radiology, and Community Health Sciences, Hotchkiss Brain Institute and Cumming School of Medicine, University of Calgary, Calgary, Alberta, Canada
  6. 6Department of Radiology, Baylor University Medical Center, Dallas, Texas, USA
  7. 7Department of NeuroInterventional Radiology, Abbott Northwestern Hospital, Minneapolis, Minnesota, USA
  8. 8Department of Radiology, University of Tennessee Medical Center, Knoxville, Tennessee, USA
  9. 9Departments of Medical Imaging and Surgery, Toronto Western Hospital, Toronto, Ontario, Canada
  10. 10Departments of Radiology and Neurosurgery, Northwestern University, Chicago, Illinois, USA
  11. 11Department of Neurology, Grady Memorial Hospital, Atlanta, Georgia, USA
  12. 12Emory University, Atlanta, Georgia, USA
  13. 13Department of Radiology, University of Massachusetts Medical School, New England Center for Stroke Research, Worcester, Massachusetts, USA
  14. 14Departments of Radiology and Neurosurgery, Carilion Clinic, Roanoke, Virginia, USA
  15. 15Department of Dermatology, Mayo Clinic, Rochester, Minnesota, USA
  16. 16Department of Neurosurgery, Mayo Clinic, Rochester, Minnesota, USA
  1. Correspondence to Dr Oana Madalina Mereuta, Department of Radiology, Mayo Clinic, Rochester, Minnesota, USA; oanamadalina.mereuta{at}nuigalway.ie

Abstract

Background Several animal studies have demonstrated that mechanical thrombectomy (MT) for acute ischemic stroke (AIS) may cause vessel wall injury (VWI). However, the histological changes in human cerebral arteries following MT are difficult to determine.

Objective To investigate the occurrence of VWI during MT by histological and immunohistochemical evaluation of AIS clots.

Methods As part of the multicenter STRIP registry, 277 clots from 237 patients were analyzed using Martius Scarlett Blue stain and immunohistochemistry for CD34 (endothelial cells) and smooth muscle actin (smooth muscle cells).

Results MT devices used were aspiration catheters (100 cases), stentriever (101 cases), and both (36 cases). VWI was found in 33/277 clots (12%). There was no significant correlation between VWI and MT device. The degree of damage varied from grade I (mild intimal damage, 24 clots), to grade II (relevant intimal and subintimal damage, 3 clots), and III (severe injury, 6 clots). VWI clots contained significantly more erythrocytes (p=0.006*) and less platelets/other (p=0.005*) than non-VWI clots suggesting soft thrombus material.

Thrombolysis correlated with a lower rate of VWI (p=0.04*). VWI cases showed a significantly higher number of passes (2 [1–4] vs 1 [1–3], p=0.028*) and poorer recanalization outcome (p=0.01*) than cases without VWI.

Conclusions Histological markers of VWI were present in 12% of AIS thrombi, suggesting that VWI might be related to MT. VWI was associated with soft thrombus consistency, higher number of passes and poorer revascularization outcome. There was no significant correlation between VWI and MT device.

  • thrombectomy
  • stroke
  • vessel wall

Data availability statement

Data are available from the corresponding author upon reasonable request.

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Data availability statement

Data are available from the corresponding author upon reasonable request.

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Footnotes

  • Twitter @FitzSeanT, @AlmekhlafiMa, @VitorMendesPer1, @PouyaNazari5, @diogohaussen, @pisanileonardo

  • OMM and MA contributed equally.

  • Contributors OMM and MA contributed equally to this study. OMM, MA, and WB were involved in all stages of the manuscript from concept design to drafting the manuscript. SF, DD, and RK were responsible for collecting and recording the clinical and procedural information from patients and were involved in the histological analysis of clots. This study is the result of a multicenter registry requiring the collaboration of multiple neurointerventionalists, research fellows, and histopathologists and all authors meet the ICJME criteria for authorship. All authors reviewed, edited, and approved the final manuscript prior to submission.

  • Funding This work was supported by the National Institutes of Health (R01 NS105853) and the European Regional Development Fund and Science Foundation Ireland (grant number 13/RC/2073).

  • Competing interests RK reports NIH funding (R01 NS076491, R43 NS110114, and R44 NS107111), is a research consultant for Cerenovus, Insera Therapeutics LLC, Marblehead Medical LLC, Microvention Inc, MIVI Neuroscience Inc, Neurogami Medical Inc, and Triticum Inc, and has stock in Neurosigma Inc (money paid to institution). AJY receives research support from Medtronic, Cerenovus, Penumbra, and Stryker, and is a consultant for Penumbra, Cerenovus, Zoll Circulation, and Vesalio. He is on the Scientific Advisory Board of XCath and Nico-lab, and has equity interest in Insera Therapeutics LLC. JEDA declares competing interests in the form of employment (modest compensation) from Medtronic and Penumbra. AMD received honoraria from Medtronic for continuing medical education events.RGN declares competing interests in the form of Stryker (DAWN Trial (DWI or CTP Assessment With Clinical Mismatch in the Triage of Wake-Up and Late Presenting Strokes Undergoing Neurointervention With TREVO) principal investigator, no compensation; TREVO Registry Steering Committee, no compensation; TREVO-2 Trial principal investigator, modest compensation; consultant, modest compensation), Medtronic (SWIFT Trial (The Solitaire With the Intention for Thrombectomy) Steering Committee, modest compensation; SWIFT-Prime Trial Steering Committee, no compensation; STAR Trial (Solitaire FR Thrombectomy for Acute Revascularisation) Angiographic Core Lab, significant compensation), Penumbra (no compensation), Cerenovus/Neuravi (ENDOLOW Trial principal investigator, EXCELLENT Registry principal investigator, ARISE-2 Trial (Analysis of Revascularization in Ischemic Stroke With EmboTrap) Steering Committee, no compensation; Physician Advisory Board, modest compensation), Phenox (Physician AdvisoryBoard, modest compensation), Anaconda (Physician Advisory Board, modest compensation), Genentech (Physician Advisory Board, modest compensation), Biogen (Physician Advisory Board, modest compensation), Prolong Pharmaceuticals (Physician Advisory Board, modest compensation), IschemaView (speaker, modest compensation), Brainomix (Research Software Use, no compensation), Sensome (Research Device Use, no compensation), Viz-AI (Physician Advisory Board, stock options), Philips (Research Software Use, no compensation; speaker, modest compensation), and Corindus Vascular Robotics (Physician Advisory Board, stock options).DFK is president of Marblehead Medical and has patent pending in balloon catheter technologies, and receives research support from Cerenovus, Insera Therapeutics LLC, Medtronic, MicroVention, MIVI Neuroscience Inc, NeuroSave, Neurogami Medical Inc, Sequent Medical and Insera, and has stock in Neurosigma Inc (money paid to institution). He is on the Scientific Advisory Board of Triticum and previously served on a SAB for Boston Scientific.WB is CMO of Marblehead Medical and has a patent pending in balloon catheter technologies, and he is a consultant for Cerenovus and Microvention. He reports NIH funding (R01 NS105853). The other authors report no conflicts.

  • Provenance and peer review Not commissioned; externally peer reviewed.

  • Supplemental material This content has been supplied by the author(s). It has not been vetted by BMJ Publishing Group Limited (BMJ) and may not have been peer-reviewed. Any opinions or recommendations discussed are solely those of the author(s) and are not endorsed by BMJ. BMJ disclaims all liability and responsibility arising from any reliance placed on the content. Where the content includes any translated material, BMJ does not warrant the accuracy and reliability of the translations (including but not limited to local regulations, clinical guidelines, terminology, drug names and drug dosages), and is not responsible for any error and/or omissions arising from translation and adaptation or otherwise.

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